Plasma Membrane Surface Potential: Dual Effects upon Ion Uptake and Toxicity

Abstract

Electrical properties of plasma membranes (PMs), partially controlled by the ionic composition of the exposure medium, play significant roles in the distribution of ions at the exterior surface of PMs and in the transport of ions across PMs. The effects of coexisting cations (commonly Al 3+ , Ca 2+ , Mg 2+ , H + , and Na + ) on the uptake and toxicity of these and other ions (such as Cu 2+ , Zn 2+ , Ni 2+ , Cd 2+ , and H 2 AsO 4 -) to plants were studied in terms of the electrical properties of PMs. Increased concentrations of cations or decreased pH in rooting media, whether in solution culture or in soils, reduced the negativity of the electrical potential at the PM exterior surface (c 0 o ). This reduction decreased the activities of metal cations at the PM surface and increased the activities of anions such as H 2 AsO 4 -. Furthermore, the reduced c 0 o negativity increased the surface-to-surface transmembrane potential difference, thus increasing the electrical driving force for cation uptake and decreasing the driving force for anion uptake across PMs. Analysis of measured uptake and toxicity of ions using electrostatic models provides evidence that uptake and toxicity are functions of the dual effects of c 0 o (i.e. altered PM surface ion activity and surface-to-surface transmembrane potential difference gradient). This study provides novel insights into the mechanisms of plant-ion interactions and extends current theory to evaluate ion bioavailability and toxicity, indicating its potential utility in risk assessment of metal(loid)s in natural waters and soils.Some solutes in growth media, such as cations and organic matter, influence the bioavailability and toxicity of metals in natural waters and soils (Peijnenburg et al., 1997;Weng et al., 2004;Kopittke et al., 2010). Novel insights into the bioavailability and toxicity of metals have inspired the development of models in order to allow accurate impact assessments of metals emitted into the environment. The biotic ligand model (BLM; Di Toro et al., 2001), as an extension of the free ion activity model (FIAM), incorporates site-specific competitions among cations (commonly Ca 2+ , Mg 2+ , and H + ) and ionic toxicants (commonly heavy metals) for binding to a biotic ligand at the cell surface. The scientific and regulatory communities have become interested in the BLM and have incorporated it into regulations. However, the BLM as the main determinant of toxicant bioavailability does not deserve uncritical acceptance, and the mechanism of the ameliorative effectiveness of cations must be considered carefully, especially in light of cation enhancement of anion toxicity (Kinraide, 2006). Previous studies (Kinraide, 2006;Wang et al., 2008) showed that global electrostatic interactions at the plasma membrane (PM) exterior surfaces, rather than site-specific mechanisms, may play the dominant role in the phytotoxicity of metals.The process of metal uptake typically encompasses diffusion of the ion to the cell surface, speciation reactions, electrostatic interac...

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